PKCθ signaling is required for myoblast fusion by regulating the expression of caveolin-3 and β1D integrin upstream focal adhesion kinase

Molecular Biology of the Cell

Volumn 22, Issue 8, 2011, Pages 1409-1419

  Madaro, Luca ^a   Marrocco, Valeria ^a   Fiore, Piera ^a   Aulino, Paola ^a   Smeriglio, Piera ^a,b   Adamo, Sergio ^a   Molinaro, Mario ^a   Bouché, Marina ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; BETA1D INTEGRIN; CAVEOLIN 3; FOCAL ADHESION KINASE; MYOGENIN; PROTEIN KINASE C THETA; TRANSCRIPTION FACTOR PAX7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CELL GROWTH; CELL NUCLEUS; COLD INJURY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE INACTIVATION; IN VITRO STUDY; MALE; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MUTANT; MYOBLAST; MYOTUBE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SATELLITE CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION; WILD TYPE;

ANIMALS; CAVEOLIN 3; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL FUSION; CELLS, CULTURED; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; INTEGRIN BETA CHAINS; MALE; MICE; MICE, KNOCKOUT; MUSCLE DEVELOPMENT; MYOBLASTS; MYOGENIN; PAX7 TRANSCRIPTION FACTOR; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; REGENERATION; SIGNAL TRANSDUCTION; STEM CELLS;

MUS; VERTEBRATA;

EID: 79954602263     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-10-0821     Document Type: Article

References (42)

1. Abmayr SM, Balagopalan L, Galletta BJ, Hong SJ (2003). Cell and molecular biology of myoblast fusion. Int Rev Cytol 225, 33-89. (Pubitemid 36443443)
2. Aulino P et al. (2010). Molecular, cellular and physiological characterization of the cancer cachexia-inducing C26 colon carcinoma in mouse. BMC Cancer 10, 363.
3. Beierle EA, Ma X, Stewart J, Nyberg C, Trujillo A, Cance WG, Golubovskaya VM (2010). Inhibition of focal adhesion kinase decreases tumor growth in human neuroblastoma. Cell Cycle 9, 1005-1015.
4. Belkin AM, Zhidkova NI, Balzac F, Altruda F, Tomatis D, Maier A, Tarone G, Koteliansky VE, Burridge K (1996). Beta 1D integrin displaces the beta 1A isoform in striated muscles: Localization at junctional structures and signaling potential in nonmuscle cells. J Cell Biol 132, 211-226.
5. Boschelli DH (2009). Small molecule inhibitors of PKCTheta as potential antiinflammatory therapeutics. Curr Top Med Chem 9, 640-654.
6. Castaldi L et al. (2007). Bisperoxovanadium, a phospho-tyrosine phos-phatase inhibitor, reprograms myogenic cells to acquire a pluripotent, circulating phenotype. FASEB J 21, 3573-3583. (Pubitemid 350075147)
7. Connors WL, Jokinen J, White DJ, Puranen JS, Kankaanpaa P, Upla P, Tulla M, Johnson MS, Heino J (2007). Two synergistic activation mechanisms of alpha2beta1 integrin-mediated collagen binding. J Biol Chem 282, 14675-14683. (Pubitemid 47100482)
8. D'Andrea M, Pisaniello A, Serra C, Senni MI, Castaldi L, Molinaro M, Bouche M (2006). Protein kinase C theta cooperates with calcineurin in the ac-tivation of slow muscle genes in cultured myogenic cells. J Cell Physiol 207, 379-388.
9. Disatnik MH, Boutet SC, Lee CH, Mochly-Rosen D, Rando TA (2002). Sequential activation of individual PKC isozymes in integrin-mediated muscle cell spreading: A role for MARCKS in an integrin signaling path-way. J Cell Sci 115, 2151-2163. (Pubitemid 34746381)
10. Disatnik MH, Boutet SC, Pacio W, Chan AY, Ross LB, Lee CH, Rando TA (2004). The bi-directional translocation of MARCKS between membrane and cytosol regulates integrin-mediated muscle cell spreading. J Cell Sci 117, 4469-4479. (Pubitemid 39360073)
11. Disatnik MH, Rando TA (1999). Integrin-mediated muscle cell spreading. The role of protein kinase c in outside-in and inside-out signaling and evidence of integrin cross-talk. J Biol Chem 274, 32486-32492.
12. Galbiati F, Volonte D, Engelman JA, Scherer PE, Lisanti MP (1999). Targeted down-regulation of caveolin-3 is sufficient to inhibit myotube forma-tion in differentiating C2C12 myoblasts. Transient activation of p38 mitogen-activated protein kinase is required for induction of caveolin-3 expression and subsequent myotube formation. J Biol Chem 274, 30315-30321.
13. Gao Z et al. (2007). Inactivation of PKCtheta leads to increased susceptibility to obesity and dietary insulin resistance in mice. Am J Physiol Endocrinol Metab 292, E84-E91. (Pubitemid 46052929)
14. Gullberg D (2003). Cell biology: The molecules that make muscle. Nature 424, 138-140. (Pubitemid 36858673)
15. Haimovich B, Kaneshiki N, Ji P (1996). Protein kinase C regulates tyrosine phosphorylation of pp125FAK in platelets adherent to fibrinogen. Blood 87, 152-161. (Pubitemid 26011829)
16. Hilgenberg L, Yearwood S, Milstein S, Miles K (1996). Neural influence on protein kinase C isoform expression in skeletal muscle. J Neurosci 16, 4994-5003. (Pubitemid 26269660)
17. Holterman CE, Rudnicki MA (2005). Molecular regulation of satellite cell function. Semin Cell Dev Biol 16, 575-584. (Pubitemid 41247881)
18. Horsley V, Jansen KM, Mills ST, Pavlath GK (2003). IL-4 acts as a myo-blast recruitment factor during mammalian muscle growth. Cell 113, 483-494. (Pubitemid 36588751)
19. Horsley V, Pavlath GK (2004). Forming a multinucleated cell: Molecules that regulate myoblast fusion. Cells Tissues Organs 176, 67-78. (Pubitemid 38199420)
20. Kuang S, Rudnicki MA (2008). The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14, 82-91.
21. Le GF, Rudnicki MA (2007). Skeletal muscle satellite cells and adult myogen-esis. Curr Opin Cell Biol 19, 628-633. (Pubitemid 350216420)
22. Lluri G, Jaworski DM (2005). Regulation of TIMP-2, MT1-MMP, and MMP-2 expression during C2C12 differentiation. Muscle Nerve 32, 492-499. (Pubitemid 41395982)
23. Lluri G, Langlois GD, Soloway PD, Jaworski DM (2008). Tissue inhibitor of metalloproteinase-2 (TIMP-2) regulates myogenesis and beta1 integrin expression in vitro. Exp Cell Res 314, 11-24. (Pubitemid 350182445)
24. Manicassamy S, Gupta S, Sun Z (2006). Selective function of PKC-theta in T cells. Cell Mol Immunol 3, 263-270.
25. Messina G et al. (2010). Nfix regulates fetal-specific transcription in develop-ing skeletal muscle. Cell 140, 554-566.
26. Mitchell KJ, Pannerec A, Cadot B, Parlakian A, Besson V, Gomes ER, Marazzi G, Sassoon DA (2010). Identification and characterization of a nonsatel-lite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12, 257-266.
27. Moraczewski J, Nowotniak A, Wrobel E, Castagna M, Gautron J, Martelly I (2002). Differential changes in protein kinase C associated with re-generation of rat extensor digitorum longus and soleus muscles. Int J Biochem Cell Biol 34, 938-949. (Pubitemid 34499592)
28. Mostafavi-Pour Z, Askari JA, Parkinson SJ, Parker PJ, Ng TT, Humphries MJ (2003). Integrin-specific signaling pathways controlling focal adhesion formation and cell migration. J Cell Biol 161, 155-167. (Pubitemid 36459088)
29. Osada S, Mizuno K, Saido TC, Suzuki K, Kuroki T, Ohno S (1992). A new member of the protein kinase C family, nPKC theta, predominantly expressed in skeletal muscle. Mol Cell Biol 12, 3930-3938.
30. Paoletti R, Maffei A, Madaro L, Notte A, Stanganello E, Cifelli G, Carullo P, Molinaro M, Lembo G, Bouche M (2010). Protein kinase C theta is required for cardiomyocyte survival and cardiac remodeling. Cell Death Dis 1, e45-doi:10.1038/cddis.2010.24. Published online 27 May 2010.
31. Pavlath GK, Horsley V (2003). Cell fusion in skeletal muscle-central role of NFATC2 in regulating muscle cell size. Cell Cycle 2, 420-423.
32. Pfeifhofer C, Kofler K, Gruber T, Tabrizi NG, Lutz C, Maly K, Leitges M, Baier G (2003). Protein kinase C theta affects Ca2+ mobilization and NFAT cell activation in primary mouse T cells. J Exp Med 197, 1525-1535. (Pubitemid 36682549)
33. Quach NL, Biressi S, Reichardt LF, Keller C, Rando TA (2009). Focal adhe-sion kinase signaling regulates the expression of caveolin 3 and beta1 integrin, genes essential for normal myoblast fusion. Mol Biol Cell 20, 3422-3435.
34. Serra C et al. (2003). Transgenic mice with dominant negative PKC-theta in skeletal muscle: A new model of insulin resistance and obesity. J Cell Physiol 196, 89-97. (Pubitemid 36676446)
35. Sun Z et al. (2000). PKC-theta is required for TCR-induced NF-kappaB acti-vation in mature but not immature T lymphocytes. Nature 404, 402-407. (Pubitemid 30164343)
36. Tigges U, Koch B, Wissing J, Jockusch BM, Ziegler WH (2003). The F-actin cross-linking and focal adhesion protein filamin A is a ligand and in vivo substrate for protein kinase C alpha. J Biol Chem 278, 23561-23569. (Pubitemid 36830176)
37. Tokugawa S, Sakuma K, Fujiwara H, Hirata M, Oda R, Morisaki S, Yasuhara M, Kubo T (2009). The expression pattern of PKCtheta in satellite cells of normal and regenerating muscle in the rat. Neuropathology 29, 211-218.
38. Tulla M, Helenius J, Jokinen J, Taubenberger A, Muller DJ, Heino J (2008). TPA primes alpha2beta1 integrins for cell adhesion. FEBS Lett 582, 3520-3524.
39. Villunger A et al. (1999). Synergistic action of protein kinase C theta and calcineurin is sufficient for Fas ligand expression and induction of a crmA-sensitive apoptosis pathway in Jurkat T cells. Eur J Immunol 29, 3549-3561. (Pubitemid 29527802)
40. Vuori K, Ruoslahti E (1993). Activation of protein kinase C precedes alpha 5 beta 1 integrin-mediated cell spreading on fibronectin. J Biol Chem 268, 21459-21462. (Pubitemid 23320625)
41. White RB, Bierinx AS, Gnocchi VF, Zammit PS (2010). Dynamics of muscle fi-bre growth during postnatal mouse development. BMC Dev Biol 10, 21.
42. Zappelli F, Willems D, Osada S, Ohno S, Wetsel WC, Molinaro M, Cossu G, Bouche M (1996). The inhibition of differentiation caused by TGFbeta in fetal myoblasts is dependent upon selective expression of PKCtheta: A possible molecular basis for myoblast diversification during limb histo-genesis. Dev Biol 180, 156-164. (Pubitemid 26426166)